Single-cell transcriptomics reveals the brain evolution of web-building spiders

Abstract

Spiders are renowned for their efficient capture of flying insects using intricate aerial webs. How the spider nervous systems evolved to cope with this specialized hunting strategy and various environmental clues in an aerial space remains unknown. Here we report a brain-cell atlas of >30,000 single-cell transcriptomes from a web-building spider (Hylyphantes graminicola). Our analysis revealed the preservation of ancestral neuron types in spiders, including the potential coexistence of noradrenergic and octopaminergic neurons, and many peptidergic neuronal types that are lost in insects. By comparing the genome of two newly sequenced plesiomorphic burrowing spiders with three aerial web-building spiders, we found that the positively selected genes in the ancestral branch of web-building spiders were preferentially expressed (42%) in the brain, especially in the three mushroom body-like neuronal types. By gene enrichment analysis and RNAi experiments, these genes were suggested to be involved in the learning and memory pathway and may influence the spiders’ web-building and hunting behaviour. Our results provide key sources for understanding the evolution of behaviour in spiders and reveal how molecular evolution drives neuron innovation and the diversification of associated complex behaviours.

RERconverge Expansion: Using Relative Evolutionary Rates to Study Complex Categorical Trait Evolution

“…There are a variety of methods applied to detect convergent evolution at the same individual nucleotides (Hasselmann et al 2008), individual amino acids (Rey et al 2018; Thomas and Hahn 2015; Fukushima and Pollock 2023), regulatory elements (Partha et al 2017; Kowalczyk, Chikina, and Clark 2022; Kaplow et al 2023; Yan et al 2023), and genes (Kosakovsky Pond et al 2020; Kowalczyk et al 2019). These methods have been applied to identify convergent molecular evolution associated with a wide variety of traits in a wide number of clades (Yusuf et al 2023; Jin et al 2023).…”